Some Properties of Royal Jelly a Functional Beekeeping Product and its Health Effects

Year 2023, , 138 - 152, 19.05.2023

Gülizar Mutlu , Doğa Akbulut , Nurten Seha Aydın , Ceren Mutlu

https://doi.org/10.31467/uluaricilik.1275691

Abstract

Royal jelly, secreted from the hypopharyngeal and mandibular glands of worker honeybees, is a natural beekeeping product with a whitish colour, distinctive odour, sour-sweet taste, and viscous structure. It has a high nutritional value because it contains various carbohydrates, proteins, essential amino acids, lipids, fatty acids, B group vitamins, vitamins A, C, D, and E, and minerals such as potassium, calcium, sodium, magnesium, and phenolic compounds. It has antimicrobial, antioxidant, antiinflammatory, antidiabetic, anticancer, and antihypertensive effects and many positive effects on the immune, nervous, and digestive systems because of its rich bioactive contents. For this reason, its consumption is preferred by society as a supplementary food and can be consumed directly in the form of royal jelly or honey, pollen, or propolis mixtures. This study was carried out to review information about some physical, sensorial, and chemical properties of royal jelly, its effects on health, and its consumption as a food.

Keywords

Royal jelly, royalisin, 10-HDA, antimicrobial, antidiabetic

FONKSİYONEL BİR ARICILIK ÜRÜNÜ OLAN ARI SÜTÜNÜN BAZI ÖZELLİKLERİ ve SAĞLIK ÜZERİNE ETKİLERİ

Abstract

İşçi bal arılarının hipofaringeal ve mandibular bezlerinden salgılanan arı sütü beyazımsı renkte, kendine özgü kokuda, ekşimsi tatlı bir tatta ve viskoz yapıda olan doğal bir arıcılık ürünüdür. Yapısında çeşitli karbonhidratlar, proteinler, esansiyel aminoasitler, lipitler, yağ asitleri, B grubu vitaminleri ile A, C, D ve E vitaminleri, potasyum, kalsiyum, sodyum, magnezyum gibi mineraller ve fenolik bileşikler bulunması nedeniyle arı sütünün besin değeri yüksektir. Arı sütünün sahip olduğu bu zengin biyoaktif bileşik içeriği sayesinde antimikrobiyal, antioksidan, antiinflamatuar, antidiyabetik, antikanser ve antihipertansif etkiler ile bağışıklık, sinir ve sindirim sistemleri üzerine birçok olumlu etkileri bulunmaktadır. Bu nedenle toplumun farklı kesimleri tarafından doğrudan arı sütü şeklinde veya bal, polen veya propolis karışımları halinde takviye gıda olarak tüketimi tercih edilmektedir. Bu çalışma arı sütünün bazı fiziksel, duyusal ve kimyasal özellikleri, sağlık üzerine etkileri ve gıda olarak tüketimi ile ilgili bilgilerin derlenmesi amacıyla gerçekleştirilmiştir.

Keywords

Arı sütü, royalisin, 10-HDA, antimikrobiyal, antidiyabetik

References

• Abandansari RM, Parsian H, Kazerouni F, Porbagher R, Zabihi E, Rahimipour A. Effect of simultaneous treatment with royal jelly and doxorubicin on the survival of the prostate cancer cell line (PC3): an in vitro study. Int J Cancer Manag, 2018, 11: e13780.
• Abdelsalam HM, Diab AA, Hussien AG, Helmi SM, Aziz JA. Ginseng and royal jelly diminish diabetic hepato-and nephrotoxicity in STZ-induced diabetic male rats. Nutrire, 2023, 48(1): 8.
• Abu-Serie MM, Habashy NH. Two purified proteins from royal jelly with in vitro dual anti-hepatic damage potency: Major royal jelly protein 2 and its novel isoform X1. Int J Biol Macromol, 2019, 128: 782-795.
• Ahmad S, Campos MG, Fratini F, Altaye SZ, Li J. New insights into the biological and pharmaceutical properties of royal jelly. Int J Mol Sci, 2020, 21(2): 382.
• Alnomasy SF, Al Shehri ZS. Anti-cancer and cell toxicity effects of royal jelly and its cellular mechanisms against human hepatoma cells. Pharmacogn Mag, 2022, 18(79): 635-640.
• Anonim. TS 6666/2000 ve T1/2010 Arı sütü standardı. Türk Standardları Enstitüsü, 24 Haziran 2010 kabul tarihli standart, Ankara.
• Anonymous. ISO 12824 international royal jelly standard. 15/09/2016, https://standards.iteh.ai/catalog/standards/sist/59729cd3-3d97-41c6-b828-32d63f914334/iso-12824-2016.
• Altaye SZ, Meng L, Li J. Molecular insights into the enhanced performance of royal jelly secretion by a stock of honeybee (Apis mellifera ligustica) selected for increasing royal jelly production. Apidologie, 2019, 50: 436-453.
• Alu'datt MH, Rababah T, Obaidat MM, Ereifej K, Alhamad MN, Mhaidat N, Andrade JE, Johargy A, Ayadi W. Probiotics in milk as functional food: characterization and nutraceutical properties of extracted phenolics and peptides from fermented skimmed milk inoculated with royal jelly. J Food Saf, 2015, 35(4): 509-522.
• Ayna A, Tunc A, Özbolat SN, Bengü AŞ, Aykutoğlu G, Canli D, Polat R, Çiftci M, Darendelioğlu E. Anticancer, and antioxidant activities of royal jelly on HT-29 colon cancer cells andmelissopalynological analysis. Turk J Bot, 2021, 45(8): 809-819.
• Bagameri L, Baci GM, Dezmirean DS. Royal jelly as a nutraceutical natural product with a focus on its antibacterial activity. Pharmaceutics, 2022, 14(6): 1142.
• Bălan A, Moga MA, Dima L, Toma S, Elena Neculau A, Anastasiu, CV. Royal jelly-A traditional and natural remedy for postmenopausal symptoms and aging-related pathologies. Molecules, 2020, 25(14): 3291.
• Balkanska R, Mladenova E, Karadjova I. Quantification of selected trace and mineral elements in royal jelly from Bulgaria by ICP-OES and etaas. J Apic Sci, 2017, 61(2): 223-232.
• Bărnuţiu LI, Mărghitaş LA, Dezmirean DS, Mihai CM, Bobiş O. Chemical composition and antimicrobial activity of Royal Jelly-Review. Sci P Anim Sci Biotechnol, 2011, 44(2): 67-72.
• Bazeyad AY, Al-Ghamdi AA, Alattal YZ. Physicochemical characteristics of local royal jelly produced in Al-Baha region, Saudi Arabia. World J Adv Res Rev, 2022, 14: 284-292.
• Bíliková K, Mirgorodskaya E, Bukovská G, Gobom J, Lehrach H, Šimúth J. Towards functional proteomics of minority component of honeybee royal jelly: The effect of post‐translational modifications on the antimicrobial activity of apalbumin2. Proteomics, 2009, 9(8): 2131-2138.
• Caixeta DC, Teixeira RR, Peixoto LG, Machado HL, Baptista NB, de Souza AV, Vilela DD, Franci CR, Salmen Espindola, F. Adaptogenic potential of royal jelly in liver of rats exposed to chronic stress. PloS One, 2018, 13(1): e0191889.
• Chen D, Guo C, Lu W, Zhang C, Xiao C. Rapid quantification of royal jelly quality by mid-infrared spectroscopy coupled with backpropagation neural network. Food Chem, 2023, 418: 135996.
• Civelek İ. Biological activities of royal jelly: a mini-review. Anatol J Biol, 2022, 3(1): 1-8.
• Collazo N, Carpena M, Nuñez-Estevez B, Otero P, Simal-Gandara J, Prieto MA. Health promoting properties of bee royal jelly: Food of the queens. Nutrients, 2021, 13(2): 543.
• Çelik S, Gerçek YC, Özkök A, Ecem Bayram N. Organic acids and their derivatives: minor components of bee pollen, bee bread, royal jelly and bee venom. Eur Food Res Technol, 2022, 248(12): 3037-3057.
• Damico ME, Rueppell O, Shaffer Z, Han B, Raymann K. High royal jelly production does not impact the gut microbiome of honeybees. Animal Microbiome, 2021, 3(1): 1-11.
• Ecem Bayram N, Cebi N, Celik S, Gercek YC, Bayram S, Tanuğur Samancı AE, Sağdıç O, Özkök A. Turkish royal jelly: amino acid, physicochemical, antioxidant, multi-elemental, antibacterial and fingerprint profiles by analytical techniques combined with chemometrics. J Apicult Res, 2021, 60(5): 751-764.
• El-Guendouz S, Lyoussi B, Miguel MG. Insight into the chemical composition and biological properties of Mediterranean royal jelly. J Apic Res, 2020a, 59(5), 890-909.
• El-Guendouz S, Machado AM, Aazza S, Lyoussi B, Miguel MG, Mateus MC, Figueiredo, AC. Chemical characterization and biological properties of royal jelly samples from the Mediterranean area. Nat Prod Commun, 2020b, 15(2): 1934578X20908080.
• Emir M. Effect of harvesting period on chemical and bioactive properties of royal jelly from Turkey. Eur Food Sci Eng, 2020, 1(1): 9-12.
• Escamilla KIA, Ordóñez YBM, Sandoval-Peraza VM, Fernández JJA, Ancona DAB. Anti-hypertensive activity in vitro and in vivo on royal jelly produced by different diets. Emir J Food Agr, 2022, 34(1): 9-15.
• Fan P, Han B, Hu H, Wei Q, Zhang X, Meng L, Nie J, Tang X, Tian X, Zhang L, Wang L, Li J. Proteome of thymus and spleen reveals that 10-hydroxydec-2-enoic acid could enhance immunity in mice. Expert Opin Ther Targets, 2020, 24(3): 267-279.
• Fratini F, Cilia G, Mancini S, Felicioli A. Royal Jelly: An ancient remedy with remarkable antibacterial properties. Microbiol Res, 2016, 192: 130-141.
• Genç M, Aslan A. Determination of trans-10-hydroxy-2-decenoic acid content in pure royal jelly and royal jelly products by column liquid chromatography. J Chromatogr A, 1999, 839(1-2): 265-268.
• Gohari I, Khajehlandi A, Mohammadi, A. Effect of high-intensity interval training with royal jelly consumption on serum levels of glucose, insulin, and insulin resistance index of overweight and obese middle-aged men: A quasi-experimental study. Jundishapur J Chronic Dis Care, 2022, 11(4): e123363.
• Guendouz M, Haddi A, Grar H, Kheroua O, Saidi D, Kaddouri, H. Preventive effects of royal jelly against anaphylactic response in a murine model of cow’s milk allergy. Pharm Biol, 2017, 55(1): 2145-2152.
• Guo H, Kouzuma Y, Yonekura M. Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chem, 2009, 113(1): 238-245.
• Guo J, Wang Z, Chen Y, Cao J, Tian W, Ma B, Dong, Y. Active components and biological functions of royal jelly. J Funct Foods, 2021, 82: 104514.
• Hassan AAM, Elenany YE, Nassrallah A, Cheng W, Abd El-Maksoud AA. Royal jelly improves the physicochemical properties and biological activities of fermented milk with enhanced probiotic viability. LWT, 2022, 155: 112912.
• Helbing S, Lattorff HMG, Moritz RF, Buttstedt A. Comparative analyses of the major royal jelly protein gene cluster in three Apis species with long amplicon sequencing. DNA Res, 2017, 24(3): 279-287.
• Hu H, Bezabih G, Feng M, Wei Q, Zhang X, Wu F, Meng L, Fang Y, Han B, Ma C, Li J. In-depth proteome of the hypopharyngeal glands of honeybee workers reveals highly activated protein and energy metabolism in priming the Secretion of Royal Jelly*[S]. Mol Cell Proteomics, 2019, 18(4): 606-621.
• Kanelis D, Tananaki C, Liolios V, Dimou M, Goras G, Rodopoulou A, Karazafiri, E, Thrasyvoulou AA. Suggestion for royal jelly specifications. Arh Hig Rada Toksikol, 2015, 66: 275–284.
• Karaca T, Şimşek N, Uslu S, Kalkan Y, Can I, Kara A, Yörük M. The effect of royal jelly on CD3+, CD5+, CD45+ T-cell and CD68+ cell distribution in the colon of rats with acetic acid-induced colitis. Allergol Immunopathol, 2012, 40(6): 357-361.
• Kausar SH, More VR. Royal jelly: Organoleptic characteristics and physicochemical properties. Pharm Chem J, 2019, 6: 20-24.
• Khan KA, Ghramh HA, Ahmad Z, El-Niweiri MA, Ahamed Mohammed ME. Queen cells acceptance rate and royal jelly production in worker honey bees of two Apis mellifera races. PloS One, 2021,16(4): e0248593.
• Khazaei M, Ansarian A, Ghanbari E. New findings on biological actions and clinical applications of royal jelly: a review. J Diet Suppl, 2018, 15(5): 757-775.
• Kim BY, Lee KS, Jung B, Choi YS, Kim HK, Yoon HJ, Gui ZZ, Lee J, Jin BR. Honeybee (Apis cerana) major royal jelly protein 4 exhibits antimicrobial activity. J Asia-Pac Entomol, 2019, 22(1): 175-182.
• Kocot J, Kiełczykowska M, Luchowska-Kocot D, Kurzepa J, Musik I. Antioxidant potential of propolis, bee pollen, and royal jelly: possible medical application. Oxi Med Cell Longev, 2018: 7074209.
• Kohno K, Okamoto I, Sano O, Arai N, Iwaki K, Ikeda M, Kurimoto M. Royal jelly inhibits the production of proinflammatory cytokines by activated macrophages. Biosci Biotechnol Biochem, 2004, 68(1): 138-145.
• Kolayli S, Sahin H, Can Z, Yildiz O, Malkoc M, Asadov A. A member of complementary medicinal food: anatolian royal jellies, their chemical compositions, and antioxidant properties. J Evid-Based Complement Altern Med, 2016, 21(4): NP43-NP48.
• Kunugi H, Mohammed Ali A. Royal jelly and its components promote healthy aging and longevity: from animal models to humans. Int J Mol Sci, 2019, 20(19): 4662.
• Li L, Wang P, Xu,Y, Wu X, Liu X. Effect of trehalose on the physicochemical properties of freeze-dried powder of royal jelly of northeastern black bee. Coatings, 2022, 12(2): 173.
• Li XA, Huang C, Xue, Y. Contribution of lipids in honeybee (Apis mellifera) royal jelly to health. J Med Food, 2013, 16(2): 96-102.
• Maghsoudlou A, Mahoonak AS, Mohebodini H, Toldra F. Royal jelly: chemistry, storage and bioactivities. J Apic Sci, 2019, 63(1): 17-40.
• Maleki V, Jafari-Vayghan H, Saleh-Ghadimi S, Adibian M, Kheirouri S, Alizadeh M. Effects of royal jelly on metabolic variables in diabetes mellitus: A systematic review. Complement Ther Med, 2019, 43: 20-27.
• Manzo LP, de-Faria FM, Dunder RJ, Rabelo-Socca EA, Consonni SR, de Almeida ACA, Regina A, Souza-Brito ARM, Luiz-Ferreira, A. Royal jelly and its dual role in TNBS colitis in mice. Sci World J, 2015: 956235.
• Melliou E, Chinou I. Chemistry and bioactivities of royal jelly. Stud Nat Prod Chem, 2014, 43: 261-290.
• Menkovska M. The newest experience with effervescent tablets containing royal jelly as functional food on packing, dosage and synergistic action in prevention, prophylaxis and healing. J Food Process Technol, 2013, 4(10): 272.
• Miguel MG, El-Guendouz S. Volatile compounds of royal jelly. Bee Products-Chemical and Biological Properties, Springer, 2017, 191-197.
• Miyauchi-Wakuda S, Kagota S, Maruyama-Fumoto K, Wakuda H, Yamada S, Shinozuka K. Effect of royal jelly on mouse isolated ileum and gastrointestinal motility. J Med Food, 2019, 22(8): 789-796.
• Mohamed AAR, Galal AA, Elewa YH. Comparative protective effects of royal jelly and cod liver oil against neurotoxic impact of tartrazine on male rat pups brain. Acta Histochem, 2015, 117(7): 649-658.
• Mostafa RE, El-Marasy SA, Jaleel GAA, Bakeer RM. Protective effect of royal jelly against diclofenac-induced hepato-renal damage and gastrointestinal ulcerations in rats. Heliyon, 2020, 6(2): e03330.
• Mureşan CI, Dezmirean DS, Marc BD, Suharoschi R, Pop OL, Buttstedt A. Biological properties and activities of major royal jelly proteins and their derived peptides. J Funct Foods, 2022, 98: 105286.
• Nader RA, Mackieh R, Wehbe R, El Obeid D, Sabatier JM, Fajloun, Z. Beehive products as antibacterial agents: a review. Antibiotics, 2021, 10(6): 717.
• Nakaya M, Onda H, Sasaki K, Yukiyoshi A, Tachibana H, Yamada K. Effect of royal jelly on bisphenol A-induced proliferation of human breast cancer cells. Biosci Biotechnol Biochem, 2007, 71(1): 253-255.
• Nohair SFA. Antidiabetic efficacy of a honey-royal jelly mixture: Biochemical study in rats. International J Health Sci, 2021, 15(4): 4-9.
• Özkök D, Silici S. Antioxidant activities of honeybee products and their mixtures. Food Sci Biotechnol, 2017, 26: 201-206.
• Özkök A, Akbay E, Samancı A, Mayda N, Onur M. Evaluation of bioactive compounds and proliferation properties of different royal jelly samples. Prog Nutr, 2021, 23(1): e2021029.
• Pan Y, Rong Y, You M, Ma Q, Chen M, Hu F. Royal jelly causes hypotension and vasodilation induced by increasing nitric oxide production. Food Sci Nutr, 2019, 7(4): 1361-1370.
• Pavel CI, Mărghitaş LA, Bobiş O, Dezmirean DS, Şapcaliu A, Radoi I, Mădaş MN. Biological activities of royal jelly-review. Sci Pap Anim Sci Biotechnol, 2011, 44(2): 108-118.
• Peng CC, Sun HT, Lin I, Kuo PC, Li JC. The functional property of royal jelly 10-hydroxy-2-decenoic acid as a melanogenesis inhibitor. BMC Complement Altern Med, 2017, 17(1): 1-8.
• Pourmoradian S, Mahdavi R, Mobasseri M, Faramarzi E, Mobasseri M. Effects of royal jelly supplementation on glycemic control and oxidative stress factors in type 2 diabetic female: a randomized clinical trial. Chin J Integr Med, 2014, 20: 347-352.
• Ramadan MF, Al-Ghamdi A. Bioactive compounds and health-promoting properties of royal jelly: A review. J Funct Foods, 2012, 4(1): 39-52.
• Ramanathan ANKG, Nair AJ, Sugunan VS. A review on Royal Jelly proteins and peptides. J Funct Foods, 2018, 44: 255-264.
• Sabatini AG, Marcazzan GL, Caboni MF, Bogdanov S, Almeida-Muradian LBD. Quality and standardisation of royal jelly. J Apiprod Apimed Sci, 2009, 1(1): 1-6.
• Salama S, Shou Q, Abd El-Wahed AA, Elias N, Xiao J, Swillam A, Umair M, Guo Z, Dagila M, Wang K, Khalifa SAM, El-Seedi HR. Royal jelly: Beneficial properties and synergistic effects with chemotherapeutic drugs with particular emphasis in anticancer strategies. Nutrients, 2022, 14(19): 4166.
• Šedivá M, Laho M, Kohútová L, Mojžišová A, Majtán J, Klaudiny J. 10-HDA, a major fatty acid of royal jelly, exhibits pH dependent growth-inhibitory activity against different strains of Paenibacillus larvae. Molecules, 2018, 23(12): 3236.
• Shakib Khoob M, Hosseini SM, Kazemi S. In vitro and in vivo antioxidant and anticancer potentials of royal jelly for dimethylhydrazine-induced colorectal cancer in wistar rats. Oxi Med Cell Longev, 2022, 9506026.
• Shen L, Liu D, Li M, Jin F, Din M, Parnell LD, Lai CQ. Mechanism of action of recombinant Acc-royalisin from royal jelly of Asian honeybee against gram-positive bacteria. PloS One, 2012, 7(10): e47194.
• Shi JL, Liao CH, Wang ZL, Wu XB. Effect of royal jelly on longevity and memory-related traits of Apis mellifera workers. J Asia-Pac Entomol, 2018, 21(4). 1430-1433.
• Soylu P, Bayram B. Bal, propolis, arı sütü, çivanperçemi (Achillea millefolium) ve ekinezya (Echinacea paradoxa) karışımından fonksiyonel gıda üretimi, ürünün fizikokimyasal ve biyokimyasal özelliklerinin incelenmesi. Bahri
• Dağdaş Hayvancılık Araştırma Dergisi, 2020, 9(1): 25-38.
• Strant M, Yücel B, Topal E, Puscasu AM, Margaoan R, Varadi A. Use of royal jelly as functional food on human and animal health. Hayvansal Üretim, 2019, 60(2): 131-144.
• Torrijos EG, Diaz YM, Segade JMB, Brito JFF, Arias TA, Bonilla PAG, Fernandez AL, Rodríguez RG. Occupational allergic respiratory disease due to royal jelly. Ann Allergy Asthma Immunol, 2016, 117(1): 102-103.
• Viuda‐Martos M, Ruiz‐Navajas Y, Fernández‐López J, Pérez‐Álvarez JA. Functional properties of honey, propolis, and royal jelly. J Food Sci, 2008, 73(9): R117-R124.
• Xue X, Wu L, Wang K. (2017). Chemical composition of royal jelly. Bee products-chemical and biological properties. Springer, 2017, 181-190.
• Yang YC, Chou WM, Widowati DA, Lin IP, Peng CC. 10-hydroxy-2-decenoic acid of royal jelly exhibits bactericide and anti-inflammatory activity in human colon cancer cells. BMC Complement Altern Med, 2018, 18: 1-7.
• You MM, Chen YF, Pan YM, Liu YC, Tu J, Wang K, Hu FL. Royal jelly attenuates LPS-induced inflammation in BV-2 microglial cells through modulating NF-κB and p38/JNK signaling pathways. Mediators Inflamm, 2018, 7834381.
• Zahran AM, Elsayh KI, Saad K, Eloseily EM, Osman NS, Alblihed MA, Badr G, Mahmoud MH. Effects of royal jelly supplementation on regulatory T cells in children with SLE. Food Nutr Res, 2016, 60(1): 32963.